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Genetic Evidence for Extreme Polyandry and Extraordinary Sex-Role Reversal in a PipeŽ Sh Adam G

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Genetic Evidence for Extreme Polyandry and Extraordinary Sex-Role Reversal in a PipeŽ Sh Adam G doi 10.1098/rspb.2001.1841 Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipe sh Adam G. Jones1*, DeEtte Walker2 and John C. Avise2 1Department of Zoology, 3029 Cordley Hall, Oregon State University, Corvallis, OR 97331, USA 2Department of Genetics,The University of Georgia, Athens, GA 30602, USA Due to the phenomenon of male pregnancy, the ¢sh family Syngnathidae (seahorses and pipe¢shes) has historically been considered an archetypal example of a group in which sexual selection should act more strongly on females than on males. However, more recent work has called into question the idea that all species with male pregnancy are sex-role reversed with respect to the intensity of sexual selection. Furthermore, no studies have formally quanti¢ed the opportunity for sexual selection in any natural breeding assemblage of pipe¢shes or seahorses in order to demonstrate conclusively that sexual selection acts most strongly on females. Here, we use a DNA-based study of parentage in the Gulf pipe¢sh Syngnathus scovelli in order to show that sexual selection indeed acts more strongly on females than on males in this species. Moreover, the Gulf pipe¢sh exhibits classical polyandry with the greatest asymmetry in reproductive roles (as quanti¢ed by variances in mating success) between males and females yet documented in any system. Thus, the intensity of sexual selection on females in pipe¢sh rivals that of any other taxon yet studied. Keywords: mating system; microsatellites; paternity; parentage; sexual selection typhle (Berglund et al. 1988, 1989; Berglund & Rosenqvist 1. INTRODUCTION 1990, 1993; Vincent et al. 1994). Observations are consist- Male pregnancy is the rule for ¢shes of the family Syng- ent with the idea that females experience greater sexual nathidae (pipe¢shes, seahorses and sea dragons). During selection than males (Vincent et al. 1994), but we copulation, the female transfers eggs to the ventral currently have no method for translating £uctuating surface of the male, where he fertilizes and carries them operational sex ratios into a metric of sexual selection in until hatching (Berglund et al. 1986a,b). Trivers (1972) and a way that allows quantitative comparison of sexual Williams (1975) believed that such dramatic paternal selection among taxa. investment should result in stronger sexual selection on Several other studies have described some aspects of females than on males in these species. However, recent the genetic mating systems of pipe¢sh in nature (Jones & work has called the generality of this prediction into Avise 1997a,b, 2001; Jones et al. 1999; McCoy et al. 2001), question by showing that seahorses are monogamous and but none have obtained a su¤ciently complete description appear not to be sex-role reversed with respect to the of the mating behaviour of both females and males for direction of sexual selection (Vincent et al. 1992; Vincent permitting a quantitative, comparative evaluation of the 1994; Masonjones & Lewis 1996, 2000; Jones et al. 1998; intensity of sexual selection. Thus, a current challenge is Kvarnemo et al. 2000). Moreover, a careful examination to obtain a su¤ciently complete characterization of the of the syngnathid literature shows that the opportunity natural mating system for a pipe¢sh in order to calculate for sexual selection has not been quanti¢ed for any pipe- commonly used measures of the intensity of sexual select- ¢sh in a way that shows with certainty that sexual selec- ion and compare these results to similar studies of other tion acts most strongly on females in natural populations. sex-role-reversed taxa. Studies of sexual selection in pipe¢sh have mainly An excellent candidate species for additional study of relied on laboratory studies of mating preference genetic mating patterns and sexual selection is the Gulf (Berglund et al. 1986a, 1988; Rosenqvist 1990) or genetic pipe¢sh Syngnathus scovelli. Female Gulf pipe¢sh are larger mating patterns (Jones et al. 2000a,b). Although these than males and have apparent secondary sexual laboratory-based studies have been very informative with characters, such as a deeply keeled abdomen and brilliant respect to some important aspects of the sexual selection stripes, which are absent in males (Brown 1972; Jones & process, they do not provide a de¢nitive measure of the Avise 1997a). These aspects of Gulf pipe¢sh natural history intensity of sexual selection in nature. Two studies have indicate that the females of this species experience strong examined the reproductive ecology of natural pipe¢sh sexual selection. Our goal was to use a microsatellite- populations and provide data on their sex ratios and based assessment of parentage in order to test this movement patterns throughout the breeding season hypothesis and quantify the magnitude of sex-role (Vincent et al. 1994, 1995). These observations can only be reversal for the ¢rst time, to our knowledge, in a natural translated into inferences about the nature of sexual select- population of pipe¢sh. ion when coupled with knowledge of female reproductive rates (Vincent et al. 1995). Such data are available and have been integrated with ¢eld studies only for Syngnathus 2. METHODS Gulf pipe¢sh were collected on 28 July 1996 from a site near *Author for correspondence ( [email protected]). Titusville in the intracoastal waterway on the Atlantic coast of Proc. R. Soc. Lond. B (2001) 268, 2531^2535 2531 © 2001 The Royal Society Received 8 June 2001 Accepted 15 August 2001 2532 A. G. Jones and others Polyandry and extraordinary sex- role reversal in apipe¢sh of female mating success. The breeding population size was esti- 0.8 males mated using a mark^recapture framework (Jones & Avise 1997b) in which marked females were considered as those whose females genotypes appeared in the brood pouches of the 27 males. The 0.6 proportion of these genotypes appearing in our sample of adult y c n females yields an estimate of the number of breeding females in e u the population (using the Lincoln Peterson method) (Pollock q ^ e 0.4 r f et al. 1990) of 55.0 11.2 (mean s.d.). Given our estimate of the § § breeding population size, we used a Monte Carlo approach to 0.2 obtain a maximum-likelihood estimate of the distribution of female mating success (a detailed description of this approach 0 has been published elsewhere in Jones & Avise (1997b)). Females were constrained to mate with a maximum of four males (the 0 1 2 3 4 maximum number of mates observed for a female in our number of mates sample), and all possible distributions with a mean mating Figure 1. Distributions of the mating success of male and success of unity (a consequence of the 1:1 ratio of females to female Gulf pipe¢sh. pregnant males) were tested. The top 5% of simulated distribu- tions that most often recovered our observed dataset were aver- aged and used as our estimate of the distribution of female Florida. A small patch of sea grass of ca. 23 m2 in area and mating success for this breeding assemblage. We calculated the surrounded on all sides by at least 2 m of bare, sandy substrate variance in female mating success from this distribution. We ran was sampled exhaustively using a dip net. A total of 34 adult additional simulations with di¡erently sized breeding popu- males and 27 adult females were collected, frozen on dry ice lations and all results were consistent with our main conclusions and returned to the laboratory for genetic analysis. The males (e.g. the maximum-likelihood estimates of the variances in and females were measured and dissected. Ornamentation was female mating success were between 1.6 and 2.1 with population scored using an index from 1 (low intensity) to 5 (high sizes ranging from 35 to 75 females). intensity). The sexual maturity of males was con¢rmed by the presence of a well-developed brood pouch and that of females 3. RESULTS AND DISCUSSION was con¢rmed by the presence of mature ova. Each embryo carried alleles consistent with paternity (a) Microsatellite-based parentage analysis by the male in whose pouch it was found and each clutch Twenty-seven of the 34 adult males were pregnant, 21 of exhibited a maximum of two maternal alleles per locus. which carried broods that were su¤ciently developed for micro- Thus, each male apparently received eggs from a single satellite assay. The broods ranged in size from six to 31 (mean of female, the multilocus genotype of whom could be recon- 16.4) embryos and we assayed nearly every embryo (a mean of structed by subtraction of the paternal alleles from the 14 per male) using four previously described microsatellite loci genotypes of the embryos. We successfully matched the (micro11.1, micro22.3, micro25.10 and micro25.22) (Jones & adult females in our ¢eld sample to 67% of the assayed Avise 1997a). Polymerase chain reaction (PCR) was carried out broods using these reconstructed maternal genotypes. as reported elsewhere (Jones & Avise 1997a) and the PCR frag- Such a high rate of success permits an accurate estimate ments were separated and sized using an ABI377 automated of the breeding population size and the distribution of sequencer. female mating success (see ½ 2). Maternal genotypes were reconstructed from the micro- Our molecular results produced three lines of evidence satellite genotypes of the progeny by subtraction of the known indicating that females experience stronger sexual select- paternal alleles. Simulations run using GERUDsim1.0 (Jones ion than males in this population of Gulf pipe¢sh. First, 2001) showed that both our probability of detecting multiple the average number of mates per mating female was esti- maternities within a brood pouch and our probability of recon- mated to be 2.2, while the average number of mates per structing maternal genotypes correctly exceeded 0.99 for this pregnant male was exactly unity (¢gure 1).
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